Five new malformed trilobites from Cambrian and Ordovician deposits from the Natural History Museum

Injured trilobites present insight into how a completely extinct group of arthropods responded to traumatic experiences, such as failed predation and moulting complications. These specimens are therefore important for more thoroughly understanding the Paleozoic predator-prey systems that involved trilobites. To expand the record of injured trilobites, we present new examples of injured Ogygopsis klotzi and Olenoides serratus from the Campsite Cliff Shale Member of the Burgess Shale Formation (Cambrian, Miaolingian, Wuliuan), Paradoxides (Paradoxides) paradoxissimus gracilis from the Jince Formation (Cambrian, Miaolingian, Drumian), Ogygiocarella angustissima from the Llanfawr Mudstones Formation (Middle–Late Ordovician, Darriwilian–Sandbian), and Ogygiocarella debuchii from the Meadowtown Formation, (Middle–Late Ordovician, Darriwilian–Sandbian). We consider the possible origins of these malformations and conclude that most injuries reflect failed predation. Within this framework, possible predators are presented, and we uncover a marked shift in the diversity of animals that targeted trilobites in the Ordovician. We also collate other records of injured Ogygo. klotzi and Ol. serratus, and Ogygi. debuchii, highlighting that these species are targets for further understanding patterns and records of trilobite injuries.


Geological context
The Ogygopsis klotzi (NHMUK PI I 4749) and Olenoides serratus (NHMUK PI IG 4437-9) figured in this study were collected from Mount Stephen in British Columbia, Canada, in Walcott's (1908) ''Ogygopsis Shale'', Burgess Shale Formation on the mountain trail 850 m above the town of Field.This is horizon is now placed within the Campsite Cliff Shale Member, a member that also outcrops at Mount Field and the Fossil Gully Fault (Fletcher & Collins, 1998;Fletcher & Collins, 2003).The association of articulated trilobite remains and with an underlying distal wedge facies suggests the unit was deposited in a deeper water, potentially euoxic setting (further from the carbonate platform forming the Cathedral Formation palaeocliff edge; Allison & Brett, 1995).Presence of the eponym for the Pagetia bootes Subzone places the member firmly within the restricted shelf Bathyuriscus-Elrathina Zone (Fletcher & Collins, 1998).This has been correlated with the upper portion of the open-shelf Ptychagnostus praecurrens Zone of North America (Robison & Babcock, 2011) and is correlated with the later portion of the Wuliuan Stage (Miaolingian) on the global scale (Peng, Babcock & Cooper, 2012).
The Ogygiocarella angustissima (NHMUK PI OR 59206) and Ogygiocarella debuchii (NHMUK PI In 23066) figured in this study were collected from two similarly aged deposits in Wales, United Kingdom.The Ogygiocarella angustissima specimen was apparently collected from Gwern-fydd, although this seems unlikely given the regional geology and lithology of the specimen.Lectotype material preserved in identical matrix has alternatively been suggested to be derived from ''Harper's quarry'', 500 m north-west of Welfield(near Builth), likely within the Llanfawr Mudstones Formation, Builth Inlier (Hughes, 1979 and references therein, also see updated stratigraphy in Davies et al., 1997;Fortey et al., 2000).The Ogygiocarella debuchii specimen conversely originates from Betton Quarry (near Shropshire) in the upper Meadowtown Formation, Shelve Inlier.Both units are dominated by fine mudstone and siltstone, likely being deposited on a relatively deep shelf environment nearby a volcanic arc (Fortey & Owens, 1987;Davies et al., 1997;Fortey et al., 2000;Owens, 2002).Known ranges of Ogygiocarella angustissima and Ogygiocarella debuchii suggest the taxa occur in either the Hustedograptus teretiusculus and/or Nemagraptus gracilis zones at these localities.However, without more precise details regarding the exact collection horizons (and associated graptolite or other shelly fauna) it impossible to determine which precisely (Hughes, 1979;Bettley, Fortey & Siveter, 2001).Hence, the figured material likely comes from somewhere within the regional Llandeilian(Llanvirn) or Aurelucian (Caradoc) stages.This correlates with the global Darriwilian (Middle Ordovician) to Sandbian (Late Ordovician) boundary (Bettley, Fortey & Siveter, 2001;Cooper & Sadler, 2012;Goldman et al., 2023).

METHODS
Trilobite specimens within the Natural History Museum Invertebrate palaeontology collection, London were reviewed for injuries.Identified specimens were from the Campsite Cliff Shale Member of the Burgess Shale Formation, Canada; Jince Formation Czech Republic; and the Llanfawr Mudstones and Meadowtown formations, Wales, UK.These specimens were photographed under low angle LED light as stacks with a Canon EOS 600D at the NHM.Images were stacked using Helicon Focus 7 (Helicon Soft Limited)

Notes.
*Minimal values where the specimen is broken.
-Exoskeletal section is not observed for the specimen.
stacking software.Measurements of specimens were collated from the images using ImageJ (Schneider, Rasband & Eliceiri, 2012) and compiled into Table 1.

RESULTS
Ogygopsis klotzi (Rominger, 1887), NHMUK PI I 4749, Cambrian (Miaolingian, Wuliuan), Campsite Cliff Shale Member of the Burgess Shale Formation, Canada.Figs.1B and 1E.NHMUK PI I 4749 is a partial, moulted, internal exoskeletal mould with an injury on the right thoracic pleural lobe.The injury is an asymmetric 'U'-shaped indentation that truncates the 5th and 6th pleural spines by a maximum of 6.6 mm.The 5th spine shows limited pleural spine recovery, and the 6th pleural spine is rounded.
NHMUK PI OR 42440 is a mostly complete, internal exoskeletal mould with three injuries along the thorax.One on the left thoracic pleural lobe and two on the right pleural lobe.The anterior-most injury is an SSI that truncates the 1st pleural spine on the left pleural lobe by 3.3 mm (Fig. 2D).The anterior-most injury on the right pleural lobe extends across the ?8th-?10th pleural spines ( ?denote uncertainty of the segment number as the specimen is broken anteriorly) (Fig. 2B).This injury has a unique morphology.The ? 8th pleural spine is rounded and truncated by 2.4 mm and the posterior section of the ?8th segment is truncated further by 4.6 mm.The ? 9th pleural spine is truncated by 6.4 mm.The indentations on the ?8th and ?9th pleural spines form a 'W'-shape.The ? 10th pleural spine is truncated by 5.4 mm and shows rounding.The posterior-most injury on the right pleural lobe is a 'W'-shaped indentation that truncates the ?13th and ?14th pleural spines by 4.3 mm and 4.7 mm, respectively (Fig. 2C).Ogygiocarella angustissima (Salter, 1865), NHMUK PI OR 59206, Middle-Late Ordovician (Darriwilian-Sandbian), Llanfawr Mudstones Formation, Wales, UK Figure 3.
NHMUK PI OR 59206 is a mostly complete external mould that has two injuries on the right side (=left pleural lobe in life).The anterior-most injury is a 'U'-shaped indentation that truncates the 1st-3rd pleural spines by 4.7 mm (Fig. 3B, white arrows).All truncated spines show rounding, and the 3rd pleural spine shows recovery (Fig. 3B, white arrows).The posterior injury is a 'V'-shaped indentation that truncates the 5th and 6th pleural spines by 2.0 mm and 4.2 mm, respectively.Both pleural spines show rounding (Fig. 3B, black arrows).
The records collated in Table 2 represent the basis for developing a much larger dataset to explore Ogygopsis klotzi injury patterns.Documentation of injured specimens housed in other collections will expand this preliminary sample and permit the left-right behavioural asymmetry hypothesis to be re-addressed (Babcock & Robison, 1989;Babcock, 1993).Recent examination of injury patterns in Cambrian trilobites have demonstrated little evidence for injury asymmetry (Pates & Bicknell, 2019;Bicknell et al., 2022a;Bicknell et al., 2023a).However, with 80% of Ogygo.klotzi unilateral injuries being right sided, this injury distribution may indeed reflect a population-level pattern (Table 2).Illustrating this condition with a statistical dataset of one species (following Pates et al., 2017;Bicknell, Paterson & Hopkins, 2019;Bicknell et al., 2022a;Bicknell et al., 2023a;Pates & Bicknell, 2019) will uncover interesting injury patterns and represents a clear direction for exploring this topic further.

On Olenoides serratus
Predators of Olenoides serratus were similar to Ogygopsis klotzi as both species are from the Burgess Shale.It is worth considering how the Ol.serratus male mating claspers may have caused injuries (Losso & Ortega-Hernández, 2022).In modern female horseshoe crabs, males cause injuries to the medial region of during amplexus (Shuster Jr, 1982;Brockmann, 1990;Shuster Jr, 2009;Bicknell, Pates & Botton, 2018c;Das et al., 2021;Bicknell et al., 2022c).It is possible that male Ol.serratus may have caused similar medial injuries during mating.However, these reduced appendages did not produce the large, laterally located injuries documented here and in Table 3.

On Paradoxides (Paradoxides) paradoxissimus gracilis
The anterior indentations on the right pleural lobe of Paradoxides (Paradoxides) paradoxissimus gracilis (NHMUK PI OR 42440, Fig. 2B) reflect either two separate attacks that targeted the same exoskeletal region, or an additional moulting complication proximal to this injury.We suggest that both options are viable here as the posterior-most section of the injury (Fig. 2B, blue arrow) shows more recovery than anterior region.As trilobites recovered from injuries anterior to posterior (McNamara & Tuura, 2011;Zong & Bicknell, 2022), the more anterior region should show more evidence of recovery.This injured region has therefore experienced an additional traumatic event, although the exact cause is unknown.The posterior injury on the right pleural lobe (Fig. 2D) is morphologically comparable to injuries ascribed to predation (Babcock, 1993;Bicknell & Paterson, 2018) supporting the assignment of this injury to failed predation.The SSI observed on this specimen (Fig. 2D) reflects failed predation (Bicknell et al., 2022a) or a moulting complication.As P. (P.) paradoxissimus gracilis has long pleural spines, that may have been damaged while moulting, resulting in an isolated injury (Šnajdr, 1978;Conway Morris & Jenkins, 1985;Daley & Drage, 2016;Drage, 2019;Drage & Daley, 2016).This specimen highlights that more research into the moulting patterns of P. (P.) paradoxissimus gracilis may help differentiate these options.

On Ogygiocarella
The abnormal recovery and fusion of ribs in Ogygiocarella debuchii (NHMUK PI In 23066; Fig. 4) in two pygidial regions indicates two different traumatic events.The injury on the left side shows no evidence of an indentation (Fig. 4C).This suggests that a moulting complication occurred, and the ribs recovered abnormally-a condition that was propagated through subsequent moulting events.Conversely, the 'U'-shaped indentation and fused pygidial ribs on the right side (Fig. 4B) indicates a failed predation attempt that recovered abnormally.Records of injured and malformed Ogygiocarella are limited(Table 4).However, the identification of five injured specimens since 2022 (Table 4) demonstrates that Ogygiocarella, specifically Ogygi.debuchii, represents another avenue for future research into injury patterns.There is also mounting evidence to support at least three distinct arthropods groups that could have targeted Ogygiocarella as prey.(1) The Middle Ordovician (Darriwilian) Castle Bank Biota fauna (Botting et al., 2023) includes a yohoiidlike arthropod that could have attacked these trilobites using raptorial appendages (Botting et al., 2023).(2) Ordovician eurypterids-forms known from Late Ordovician(Sandbian) aged Welsh deposits (Størmer, 1951;Tetlie, 2007)-have been highlighted as possible, albeit ineffective, predators of trilobites (Lamsdell et al., 2015;Bicknell, Melzer & Schmidt, 2022b;Schmidt et al., 2022).If they were the predators, eurypterids would have targeted trilobites during a soft-shelled stage.(3) The large asaphid trilobites themselves could have targeted each other and used gnathobasic spines on walking legs to process the biomineralised exoskeletons.
Beyond arthropods, nautiloids are commonly suggested as Ordovician predators of trilobites (Brett, 2003;Klug et al., 2018).These large cephalopods would have been able to grapple trilobites with tentacles and damage the exoskeletons with re-enforced beaks (Klug et al., 2018).